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Tracking the Rising Extinction Risk of Sharks and Rays in the Northeast Atlantic Ocean and Mediterranean Sea Rachel H

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Tracking the Rising Extinction Risk of Sharks and Rays in the Northeast Atlantic Ocean and Mediterranean Sea Rachel H www.nature.com/scientificreports OPEN Tracking the rising extinction risk of sharks and rays in the Northeast Atlantic Ocean and Mediterranean Sea Rachel H. L. Walls* & Nicholas K. Dulvy The loss of biodiversity is increasingly well understood on land, but trajectories of extinction risk remain largely unknown in the ocean. We present regional Red List Indices (RLIs) to track the extinction risk of 119 Northeast Atlantic and 72 Mediterranean shark and ray species primarily threatened by overfshing. We combine two IUCN workshop assessments from 2003/2005 and 2015 with a retrospective backcast assessment for 1980. We incorporate predicted categorisations for Data Defcient species from our previously published research. The percentage of threatened species rose from 1980 to 2015 from 29 to 41% (Northeast Atlantic) and 47 to 65% (Mediterranean Sea). There are as many threatened sharks and rays in Europe as there are threatened birds, but the threat level is nearly six times greater by percentage (41%, n = 56 of 136 vs. 7%, n = 56 of 792). The Northeast Atlantic RLI declined by 8% from 1980 to 2015, while the higher-risk Mediterranean RLI declined by 13%. Larger-bodied, shallow-distributed, slow-growing species and those with range boundaries within the region are more likely to have worsening status in the Northeast Atlantic. Conversely, long- established, severe threat levels obscure any potential relationships between species’ traits and the likelihood of worsening IUCN status in the Mediterranean Sea. These regional RLIs provide the frst widespread evidence for increasing trends in regional shark and ray extinction risk and underscore that efective fsheries management is necessary to recover the ecosystem function of these predators. Overfshing is the most imminent threat to many marine organisms1. Governments need repeated comprehen- sive assessments of extinction risk to efectively monitor the status of marine biodiversity 2 and track progress towards global biodiversity and sustainable development targets 3 if they are to halt declines, prevent more local extinctions, and recover species. Te Red List Index (RLI) tracks the changing extinction risk of groups of species based on status changes recorded on the International Union for Conservation of Nature Red List of Treatened Species4 (hereafer ‘IUCN Red List’). Te RLI includes species listed under six categories, in ascending order of threat: Least Concern, Near Treatened, Vulnerable, Endangered, Critically Endangered, and Extinct, but excludes the Data Defcient category 4. Tus far, the RLI has mostly been applied to terrestrial species, including birds, mammals, amphibians, and cycads5–8. Our only understanding of changing marine extinction risk from the RLI so far comes from its application to stony corals, which reveals the threat of climate change to a key group of foundation species in the tropical oceans9. Tere remains a pressing need to develop an extinction risk trajectory representative of widely distributed marine fshes that are primarily threatened by overexploitation to better-understand the efects of this more immediate threat. Te RLI is eventually intended for global-level application, but like the Red List Assessments themselves, it is also informative when applied at regional and national scales 10 or decomposed by biome, habitat, conserva- tion profle, or international treaty 5. Here we focus on a regional Red List assessment because these fner-scale analyses better-connect species status and trajectory to local and regional variation in threats and conservation management across socio-political and economic regimes11,12. We focus on the sharks, rays, and ghost sharks (Class Chondrichthyes, herein ‘sharks and rays’) in the Northeast Atlantic Ocean and Mediterranean Sea for four reasons: (1) sharks and rays have the greatest percentage of ‘threatened’ species (i.e. Vulnerable, Endangered, or Critically Endangered) of any taxonomic Class of marine organisms13, with numerous populations worldwide already locally or regionally extinct due to overfshing1,14,15, including many from the Northeast Atlantic and Mediterranean Sea16–18; (2) the status of sharks and rays in this region has been comprehensively assessed twice: Earth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada. *email: [email protected] Scientifc Reports | (2021) 11:15397 | https://doi.org/10.1038/s41598-021-94632-4 1 Vol.:(0123456789) www.nature.com/scientificreports/ in 2003/2005 and in 201519–21; (3) the Northeast Atlantic and Mediterranean Sea may be a ‘canary-in-the-coal mine’ for collapse and recovery of fsh populations because of the combination of a long history of exploitation22, high scientifc capacity 17, substantial modern fshing efort 23, and divergent patterns of fsheries development and management24; and (4) extinction risk categorisations have already been predicted for the Data Defcient species in these regions in previous research 25, presenting the opportunity to include these Data Defcient species in the RLI as well. One of the key challenges for the development of a taxonomically representative indicator is the high number of Data Defcient species listed, which until now have been excluded from trajectories of extinction risk even though some of them are predicted to be at risk25. Here, we provide a regional synthesis of the changing extinction risk for sharks and rays in the Northeast Atlantic and Mediterranean Sea (the RLI). We retrospectively assign IUCN categorisations to each species for the year 1980 through a critical review of historical fshing patterns and scientifc literature4,7,26. In our previously published research we predicted the IUCN categorisations of all Data Defcient species in 2015 (n = 21 North- east Atlantic, n = 12 Mediterranean)25, which we now incorporate into the RLIs alongside the IUCN-assessed categorisations (n = 98 + 21 = 119 Northeast Atlantic, n = 60 + 12 = 72 Mediterranean). We disaggregate the RLIs by primary habitat, then further explore the biological and ecological traits that are related to extinction risk. We build on the knowledge that sharks and rays with slower life histories (i.e. slower growth and population turnover rates27–29) and shallower depth distributions (i.e. higher exposure to fshing activity due to limited depth refuge30) are more likely to be categorised as threatened on the IUCN Red List 25,30 by exploring the likelihood of shark and ray Red List status worsening between assessment years based on these biological and ecological traits. Results and discussion Changes in extinction risk from 1980 to 2015. We compiled the results from the frst (2003 Mediterra- nean Sea19, 2005 Northeast Atlantic 20) and second (2015 18,21) regional IUCN Red List assessments of sharks and rays, then ‘backcast’ (i.e., retrospectively assigned an IUCN status) to 1980 through a critical review of historical fshing patterns and scientifc literature4,7,26 (see Methods for further detail and Supplementary Information for species-specifc backcasting justifcations). We fnd that sharks and rays in the Northeast Atlantic and Mediterranean Sea faced elevated levels of extinc- tion risk by 1980 and since then their status has steadily worsened (Fig. 1a). Te RLI is scaled from zero to one, where zero means all species are Extinct and one means all species are Least Concern 4. In the Northeast Atlan- tic the shark and ray RLI declined from a backcast value of 0.80 in 1980 to 0.74 in 2005 and further to 0.72 in 2015 (8% decline in RLI over 35 years; Fig. 1a). To represent the potential range of index values from the group assessed, we generated a confdence interval by bootstrapping (sampling with replacement) the 1980 statuses 31 (upper and lower confdence interval 0.85–0.75). Te change in Northeast Atlantic shark and ray status equates to an average rate of decline of 0.2% year -1. Te backcast Mediterranean Sea start-point was lower by 1980 than the 2015 Northeast Atlantic end-point, refecting greater Mediterranean extinction risk. Te Mediterranean RLI declined from a backcast value of 0.67 in 1980 (upper and lower confdence interval 0.74–0.61) to 0.59 in 2003, then to 0.54 in 2015 (13% decline in RLI over 35 years; Fig. 1a). In this region, the average rate of decline was 0.4% year−1, declining from 0.3% year−1 (1980–2003) to 0.4% year −1 (2003–2015). Between 1980 and 2015, the percentage of shark and ray species listed as threatened increased by 12% in the Northeast Atlantic (Fig. 1b) and 18% in the Mediterranean Sea (Fig. 1c). Almost one-third (29%, n = 35 of 119) of Northeast Atlantic sharks and rays were backcast into threatened categories in 1980 and this fraction rose to under two-ffhs (39%, 46) by 2005 20 and subsequently to over two-ffhs (41%, 49) by 2015 25 (Fig. 1b). In the Mediterranean Sea, almost half (47%, 34 of 72) of shark and ray species were backcast as threatened in 1980, and this fraction increased to over three-ffhs (61%, 44)19 by 2003 and further to nearly two-thirds (65%, 47) in 2015 25. Te divergence in extinction risk between ocean basins is apparent in the greatest percentage of Northeast Atlantic species listings being Least Concern (57%, n = 68 in 1980 and 45%, n = 54 in 2015; Fig. 1b). Conversely, while 32% (n = 23, the greatest percentage) of Mediterranean species listings were historically Least Concern in 1980, in 2015, the same percentage (32%, n = 23, the greatest percentage) are Critically Endangered. When calculating the RLI, the high weighting given to Critically Endangered species made them a key driver of the lower RLI value in the Mediterranean Sea (Fig. 1c; see Methods for category weights). Te increasing extinction risk of Northeast Atlantic and Mediterranean sharks and rays is greater than any globally assessed vertebrate group on the RLI (Fig. 1a). Further, this risk is increasing faster than for other vertebrate lineages on the RLI: 7–9 times faster than global birds (1% decline in RLI over 26 years), 3–5 times faster than mammals (1% decline in RLI over 13 years), and 2–3 times faster than amphibians (4% decline in RLI over 26 years; Fig.
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